Pseudomonas aeruginosa Anaerobic Respiration in Biofilms

Yoon, Sang Sun; Hennigan, Robert F.; Hilliard, George M.; Ochsner, Urs A.; Parvatiyar, Michelle S.; Kamani, Moneesha C.; Allen, Holly L.; DeKievit, Teresa R.; Gardner, Paul R.; Schwab, Ute; Rowe, John J.; Iglewski, Barbara H.; McDermott, Timothy R.; Mason, Ronald P.; Wozniak, Daniel J.; Hancock, Robert E. W.; Parsek, Matthew R.; Noah, Terry L.; Boucher, Richard C.; Hassett, Daniel J.

doi:10.1016/s1534-5807(02)00295-2

Cited by 536 publications

(489 citation statements)

References 27 publications

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“…There has been recent debate on the nature of the microbial habitat in the CF lung, particularly with respect to whether conditions are aerobic or anaerobic [3,4]. Understanding lung environmental conditions is clinically important, as the efficacy of several antibiotics is dependent on the chemical milieu, i.e.…”

Section: Discussionmentioning

confidence: 99%

“…Bacterial virulence factors undoubtedly also contribute to lung damage, but they have been poorly characterised in vivo. In CF airways, P. aeruginosa is thought to grow in anaerobic/reduced oxygen pockets situated within thickened and tenacious mucus plugs that occlude small airways [3,4]. This environment may be suitable for cyanide production by P. aeruginosa [5][6][7].…”

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confidence: 99%

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Bacterial cyanogenesis occurs in the cystic fibrosis lung

Sanderson¹,

Wescombe²,

Kirov³

et al. 2008

European Respiratory Journal

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The cystic fibrosis (CF) lung environment is poorly defined, but data suggest that bacteria may encounter reduced oxygen tensions and possibly an anaerobic environment. Pseudomonas aeruginosa produces the potent toxin cyanide under strictly microaerobic conditions. Evidence of bacterial cyanogenesis in the CF lung was investigated in the present study by measuring sputum cyanide concentrations.Sputum cyanide was measured in seven stable CF patients, as well as before and after intravenous antibiotic therapy during a hospital admission in a further eight patients experiencing acute exacerbations. All patients were chronically infected with P. aeruginosa. Comparative sputum data were obtained from nine CF patients with no documented P. aeruginosa infection and 10 healthy, nonsmoking normal controls.High levels of cyanide were detected in all the P. aeruginosa-infected stable CF patients (median (range) 0.56 (0.37-2.81) mg?mL -1 ), and in seven out of eight acute sputum samples (0.73 (0-1.43) mg?mL -1 ). In contrast, cyanide was not detectable in sputum from eight out of nine CF patients without P. aeruginosa infection or in any of the normal controls. Intravenous antibiotic treatment significantly reduced sputum cyanide levels (median 0.73 to median 0.0 mg?mL -1 ).The cyanide detected indicates that the cystic fibrosis lung provides a predominantly microaerobic environment for Pseudomonas aeruginosa. Cyanide is likely to be a potentially important virulence factor in Pseudomonas aeruginosa-infected cystic fibrosis patients.

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Bacterial cyanogenesis occurs in the cystic fibrosis lung

Sanderson¹,

Wescombe²,

Kirov³

et al. 2008

European Respiratory Journal

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“…For example, PA can participate in quorum sensing, a process in which the density of organisms in a given population can alter the behavior of individual organisms within the population (34). Also, Pseudomonas species are capable of forming biofilms when enough bacteria are present, and these structures can interact with various surfaces in a unique manner when compared with interactions by unorganized populations of bacteria (35). Another possibility is that PA, in contrast to E. coli or K. pneumoniae, has the capacity to constitutively produce a substance (i.e., inhibitor) that interferes with induction of the PMN migration process and is only effective if enough PA is present to allow the accumulation of the appropriate amount of that substance.…”

Section: Discussionmentioning

confidence: 99%

Polymorphonuclear Cell Transmigration Induced by Pseudomonas aeruginosa Requires the Eicosanoid Hepoxilin A3

Hurley

Siccardi

Mrsny

et al. 2004

The Journal of Immunology

160

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Lung inflammation resulting from bacterial infection of the respiratory mucosal surface in diseases such as cystic fibrosis and pneumonia contributes significantly to the pathology. A major consequence of the inflammatory response is the recruitment and accumulation of polymorphonuclear cells (PMNs) at the infection site. It is currently unclear what bacterial factors trigger this response and exactly how PMNs are directed across the epithelial barrier to the airway lumen. An in vitro model consisting of human PMNs and alveolar epithelial cells (A549) grown on inverted Transwell filters was used to determine whether bacteria are capable of inducing PMN migration across these epithelial barriers. A variety of lung pathogenic bacteria, including Klebsiella pneumoniae, Escherichia coli, and Pseudomonas aeruginosa are indeed capable of inducing PMN migration across A549 monolayers. This phenomenon is not mediated by LPS, but requires live bacteria infecting the apical surface. Bacterial interaction with the apical surface of A549 monolayers results in activation of epithelial responses, including the phosphorylation of ERK1/2 and secretion of the PMN chemokine IL-8. However, secretion of IL-8 in response to bacterial infection is neither necessary nor sufficient to mediate PMN transepithelial migration. Instead, PMN transepithelial migration is mediated by the eicosanoid hepoxilin A3, which is a PMN chemoattractant secreted by A549 cells in response to bacterial infection in a protein kinase C-dependent manner. These data suggest that bacterial-induced hepoxilin A3 secretion may represent a previously unrecognized inflammatory mechanism occurring within the lung epithelium during bacterial infections.

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“…Given the fact that P. aeruginosa is able to grow anaerobically in the presence of alternative electron acceptors such as nitrate (NO 3 Ϫ ) or nitrite (NO 2 Ϫ ) that are present in sufficient quantity in a CF mucus layer (21,31,59), further research on bacterial responses to an anaerobic environment should be pursued for an integrated understanding of its virulence mechanisms. From this perspective, it is of particular interest that P. aeruginosa growing by anaerobic respiration forms a significantly more robust biofilm than that formed during aerobic growth, allow-ing the establishment of a resistant mode of bacterial proliferation (32,59). Moreover, bactericidal activity of polymorphonuclear neutrophils (PMN) was significantly decreased under conditions of low oxygen tension due to the impaired production of hydrogen peroxide (30).…”

mentioning

confidence: 99%

Anaerobiosis-Induced Loss of Cytotoxicity Is Due to Inactivation of Quorum Sensing in Pseudomonas aeruginosa

et al. 2011

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Pseudomonas aeruginosa, an opportunistic pathogen of clinical importance, causes chronic airway infections in patients with cystic fibrosis (CF). Current literature suggests that pockets with reduced oxygen tension exist in the CF airway mucus. However, virulence features of this opportunistic pathogen under such conditions are largely unknown. Cell-free supernatant of the standard laboratory P. aeruginosa strain PAO1 obtained from anaerobic culture, but not aerobic culture, failed to kill A549 human airway epithelial cells. Further investigation revealed that this reduced cytotoxicity upon anaerobiosis was due to the suppressed secretion of elastase, a virulence factor controlled by P. aeruginosa quorum sensing (QS). Both a lacZ-reporter fusion assay and quantitative real-time PCR (RT-PCR) analysis demonstrated that transcription of the elastase-encoding lasB gene was substantially decreased during anaerobic growth compared with aerobic growth. Moreover, transcription of other genes controlled by the LasI/R QS system, such as rhlR, vqsR, mvfR, and rsaL, was also repressed under the same anaerobic growth conditions. Importantly, synthesis of 3-oxo-C 12 -HSL (PAI-1), an autoinducer molecule that mediates induction of the LasI/R QS system, was >22-fold decreased during anaerobic growth while C 4 -HSL (PAI-2), which mediates RhlI/R QS, was nondetectable under the same growth conditions. Transcription of the lasB gene was restored by exogenous supplementation with autoinducers, with PAI-2 more effective than PAI-1 or Pseudomonas quinolone signal (PQS) at restoring transcription of the lasB gene. Together, these results suggest that anaerobiosis deprives P. aeruginosa of the ability to regulate its virulence via QS and this misregulation attenuates the pathogenic potential of this important pathogen.

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Pseudomonas aeruginosa Anaerobic Respiration in Biofilms

Cited by 536 publications

References 27 publications

Bacterial cyanogenesis occurs in the cystic fibrosis lung

Bacterial cyanogenesis occurs in the cystic fibrosis lung

Polymorphonuclear Cell Transmigration Induced by Pseudomonas aeruginosa Requires the Eicosanoid Hepoxilin A3

Anaerobiosis-Induced Loss of Cytotoxicity Is Due to Inactivation of Quorum Sensing in Pseudomonas aeruginosa

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